Light at night reduces digestive efficiency of developing birds: an experiment with king quail

Abstract

Artificial light at night (ALAN) exposes animals to a novel environmental stimulus, one that is generally thought to be maladaptive. ALAN-related health problems have received little attention in non-model species, and we generally know little about the nutritional-physiological impacts of ALAN, especially in young animals. Here, we use a novel application of the acid steatocrit method to experimentally assess changes in digestive efficiency of growing king quail (Excalfactoria chinensis) in response to ALAN. Two weeks after hatching, quail were split into two groups (n = 20–21 per group): overnight-light-treated vs. overnight-dark-treated. When the chicks were 3 weeks old, the experimental group was exposed to weak blue light (ca. 0.3 lux) throughout the entire night for 6 consecutive weeks, until all the chicks had achieved sexual maturation. Fecal samples for assessing digestive efficiency were collected every week. We found that digestive efficiency of quail was reduced by ALAN at two time points from weeks 4 to 9 after hatching (quail reach adulthood by week 9). The negative effect of ALAN on digestion coincided with the period of fastest skeletal growth, which suggests that ALAN may reduce digestive efficiency when energetic demands of growth are at their highest. Interestingly, growth rate was not influenced by ALAN. This suggests that either the negative physiological impacts of ALAN may be concealed when food is provided ad libitum, the observed changes in digestive efficiency were too small to affect growth or condition, or that ALAN-exposed birds had reduced energy expenditure. Our results illustrate that the health impacts of ALAN on wild animals should not be restricted to traditional markers like body mass or growth rate, but instead on a wide array of integrated physiological traits.

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Data for this article is available in supplementary materials.

References

  1. Alaasam VJ, Duncan R, Casagrande S, Davies S, Sidher A, Seymoure B, Shen Y, Zhang Y, Ouyang JQ (2018) Light at night disrupts nocturnal rest and elevates glucocorticoids at cool color temperatures. J Exp Zool A 329:465–472. https://doi.org/10.1002/jez.2168

    CAS  Article  Google Scholar 

  2. Apeldoorn EJ, Schrama JW, Mashaly MM, Parmentier HK (1999) Effect of melatonin and lighting schedule on energy metabolism in broiler chickens. Poultry Sci 78:223–229. https://doi.org/10.1093/ps/78.2.223

    CAS  Article  Google Scholar 

  3. Baghbanzadeh A, Decuypere E (2008) Ascites syndrome in broilers: physiological and nutritional perspectives. Avian Pathol 37:117–126. https://doi.org/10.1080/03079450801902062

    CAS  Article  PubMed  Google Scholar 

  4. Cho Y-M, Ryu S-H, Lee BR, Kim KH, Lee E, Choi J (2015) Effects of artificial light at night on human health: a literature review of observational and experimental studies applied to exposure assessment. Chronobiol Int 32:1294–1310. https://doi.org/10.3109/07420528.2015.1073158

    Article  PubMed  Google Scholar 

  5. Dominoni DM (2015) The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective. J Ornithol 156:409–418. https://doi.org/10.1007/s10336-015-1196-3

    Article  Google Scholar 

  6. Dominoni DM, Goymann W, Helm B, Partecke J (2013) Urban-likenight illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds. Front Zool 10:60. https://doi.org/10.1186/1742-9994-10-60

  7. Dominoni DM, Borniger JC, Nelson RJ (2016) Light at night, clocks and health: from humans to wild organisms. Biol Lett 12:20160015. https://doi.org/10.1098/rsbl.2016.0015

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Durrant J, Green MP, Jones TM (2019) Dim artificial light at night reduces the cellular immune response of the black field cricket, Teleogryllus commodus. Insect Sci 27:571–582. https://doi.org/10.1111/1744-7917.12665

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Falchi F, Cinzano P, Duriscoe D, Kyba CCM, Elvidge CD, Baugh K, Furgoni R (2016) The new world atlas of artificial night sky brightness. Sci Adv 2:e1600377. https://doi.org/10.1126/sciadv.1600377

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Fonken LK, Nelson RJ (2014) The effects of light at night on circadian clocks and metabolism. Endocr Rev 35:648–670. https://doi.org/10.1210/er.2013-1051

    CAS  Article  PubMed  Google Scholar 

  11. Fonken LK, Nelson RJ (2020) Effects of light exposure at night during development. Curr Opin Behav Sci 7:33–39. https://doi.org/10.1016/j.cobeha.2015.10.008

  12. Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A, Nelson RJ (2010) Light at night increases body mass by shifting the time of food intake. Proc Nat Acad Sci 107:18664–18669. https://doi.org/10.1073/pnas.1008734107

    Article  PubMed  Google Scholar 

  13. Gaston KJ, Bennie J, Davies TW, Hopkins J (2013) The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol Rev 88:912–927. https://doi.org/10.1111/brv.12036

    Article  PubMed  Google Scholar 

  14. Haraguchi S, Kamata M, Tokita T, Tashiro K, Sato M, Nozaki M et al (2019) Light-at-night exposure affects brain development through pineal allopregnanolone-dependent mechanisms. eLife 8:e45306

    Article  Google Scholar 

  15. Ingram D, Hattens L, Mcpherson B (2000) Effects of light restriction on broiler performance and specific body structure measurements. Physiol Psychol 9:501–504. https://doi.org/10.1093/japr/9.4.501

    Article  Google Scholar 

  16. Landry GP (2015) The care, breeding and genetics of the button quail, 3rd ed. Poule d’eau, Publishing Co., Franklin, Lousiana

    Google Scholar 

  17. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. The Auk 104:116–121. https://doi.org/10.2307/4087240

    Article  Google Scholar 

  18. Madonia C, Hutton P, Giraudeau M, Sepp T (2017) Carotenoid coloration is related to fat digestion efficiency in a wild bird. Sci Nat 104:96. https://doi.org/10.1007/s00114-017-1516-y

    CAS  Article  Google Scholar 

  19. Malek I, Haim A, Izhaki I (2020) Melatonin mends adverse temporal effects of bright light at night partially independent of its effect on stress responses in captive birds. Chronobiol Int 37:189–208. https://doi.org/10.1080/07420528.2019.1698590

    CAS  Article  PubMed  Google Scholar 

  20. Masís-Vargas A, Hicks D, Kalsbeek A, Mendoza J (2019) Blue light at night acutely impairs glucose tolerance and increases sugar intake in the diurnal rodent Arvicanthis ansorgei in a sex-dependent manner. Physiol Rep 7:e14257. https://doi.org/10.14814/phy2.14257

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Meitern R, Lind MA, Karu U, Hõrak P (2016) Simple and non-invasive method for assessment of digestive efficiency: validation of fecal steatocrit in greenfinch coccidiosis model. Ecol Evol 6:8756–8763. https://doi.org/10.1002/ece3.2575

    Article  PubMed  PubMed Central  Google Scholar 

  22. Mishra I, Knerr RM, Stewart AA, Payette WI, Richter MM, Ashley NT (2019) Light at night disrupts diel patterns of cytokine gene expression and endocrine profiles in zebra finch (Taeniopygia guttata). Sci Rep 9:15833. https://doi.org/10.1038/s41598-019-51791-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Motilva V, Cabeza J, Alarcon de La Lastra C (2001) New issues about melatonin and its effects on the digestive system. Curr Pharm Design 7:909–931. https://doi.org/10.2174/1381612013397681

    CAS  Article  Google Scholar 

  24. Olanrewaju HA, Miller WW, Maslin WR, Collier SD, Purswell JL, Branton SL (2015) Influence of photoperiod, light intensity and their interaction on health indices of modern broilers grown to heavy weights. Int J Poultry Sci 14:183–190. https://doi.org/10.3923/ijps.2015.183.190

    Article  Google Scholar 

  25. Ouyang JQ, Davies S, Dominoni D (2018) Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function. J Exp Biol 221:jeb156893

    Article  Google Scholar 

  26. Pearson JT, Tsudzuki M, Nakane Y, Akiyama R, Tazawa H (1998) Development of heart rate in the precocial king quail Coturnix chinensis. J Exp Biol 201:931–941

    CAS  PubMed  Google Scholar 

  27. Phuapradit P, Narang A, Mendonca P, Harris DA, Baum JD (1981) The steatocrit: a simple method for estimating stool fat content in newborn infants. Arch Dis Child 56:725–727

    CAS  Article  Google Scholar 

  28. Podkowa P, Surmacki A (2017) The importance of illumination in nest site choice and nest characteristics of cavity nesting birds. Sci Rep 7:1329. https://doi.org/10.1038/s41598-017-01430-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Raap T, Casasole G, Costantini D, AbdElgawad H, Asard H, Pinxten R, Eens M (2016a) Artificial light at night affects body mass but not oxidative status in free-living nestling songbirds: an experimental study. Sci Rep 6:35626. https://doi.org/10.1038/srep35626

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Raap T, Casasole G, Pinxten R, Eens M (2016b) Early life exposure to artificial light at night affects the physiological condition: an experimental study on the ecophysiology of free-living nestling songbirds. Environ Pollut 218:909–914. https://doi.org/10.1016/j.envpol.2016.08.024

    CAS  Article  PubMed  Google Scholar 

  31. Raap T, Pinxten R, Eens M (2018) Artificial light at night causes an unexpected increase in oxalate in developing male songbirds. Conserv Physiol 6:coy005. https://doi.org/10.1093/conphys/coy005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Rich C, Longcore T (2007) Ecological consequences of artificial night lighting. Island Press, Washington, DC

    Google Scholar 

  33. Rybnikova NA, Haim A, Portnov BA (2016) Does artificial light-at-night exposure contribute to the worldwide obesity pandemic? Int J Obesity 40:815–823. https://doi.org/10.1038/ijo.2015.255

    CAS  Article  Google Scholar 

  34. Saini C, Hutton P, Gao S, Simpson RK, Giraudeau M, Sepp T, Webb E, McGraw KJ (2019) Exposure to artificial light at night increases innate immune activity during development in a precocial bird. Comp Biochem Phys A 233:84–88. https://doi.org/10.1016/j.cbpa.2019.04.002

    CAS  Article  Google Scholar 

  35. Salmón P, Nilsson JF, Nord A, Bensch S, Isaksson C (2016) Urban environment shortens telomere length in nestling great tits, Parus major. Biol Lett 12:20160155. https://doi.org/10.1098/rsbl.2016.0155

  36. Sanders D, Gaston KJ (2018) How ecological communities respond to artificial light at night. J Exp Zool A 329:394–400. https://doi.org/10.1002/jez.2157

    Article  Google Scholar 

  37. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass–size residuals: validating body condition indices. Ecology 86:155–163. https://doi.org/10.1890/04-0232

    Article  Google Scholar 

  38. Schwean-Lardner K, Fancher BI, Gomis S, Van Kessel A, Classen HL (2013) Effect of day length on cause of mortality, leg health and ocular health in broilers. Poult Sci 92:1–11. https://doi.org/10.3382/ps.2011-01967

    CAS  Article  PubMed  Google Scholar 

  39. Svechkina A, Portnov BA, Trop T (2020) The impact of artificial light at night on human and ecosystem health: a systematic literature review. Landscape Ecol 35:1725–1742. https://doi.org/10.1007/s10980-020-01053-1

    Article  Google Scholar 

  40. Ulgezen ZN, Käpylä T, Meerlo P, Spoelstra K, Visser ME, Dominoni DM (2019) The preference and costs of sleeping under light at night in forest and urban great tits. Proc R Soc B 28620190872:20190872. https://doi.org/10.1098/rspb.2019.0872

    Article  Google Scholar 

  41. Welbers AAMH, van Dis NE, Kolvoort AM, Ouyang J, Visser ME, Spoelstra K, Dominoni DM (2017) Artificial light at night reduces daily energy expenditure in breeding great tits (Parus major). Front Ecol Evol doi 5. https://doi.org/10.3389/fevo.2017.00055

  42. Yang YF, Jin SF, Zhong ZT, Yu YH, Yang B, Yuan HB, Pan JM (2015) Growth responses of broiler chickens to different periods of artificial light. J Animal Sci 93:767–775

    CAS  Article  Google Scholar 

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Acknowledgments

We thank Devon Allred and Arizona State University Department of Animal Care and Technologies staff for help with bird maintenance.

Funding

This work was supported by the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement no. 701747 and the Estonian Research Council (IUT34-8, PSG458).

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Correspondence to Tuul Sepp.

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The authors declare that they have no conflict of interest.

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This study was carried out with the approval of Arizona State University’s IACUC and complies with the National Institutes of Health guidelines for the care and use of laboratory animals.

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Communicated by: Matthias Waltert & Paula Roig Boixeda

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Sepp, T., Webb, E., Simpson, R.K. et al. Light at night reduces digestive efficiency of developing birds: an experiment with king quail. Sci Nat 108, 4 (2021). https://doi.org/10.1007/s00114-020-01715-9

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Keywords

  • Steatocrit
  • Light pollution
  • Development
  • Avian
  • Digestion
  • Excalfactoria chinensis